LFA-1 activity state on dendritic cells regulates contact duration with T cells and promotes T-cell priming

Blood

Volumn 116, Issue 11, 2010, Pages 1885-1894

  Balkow, Sandra ^a   Heinz, Stefanie ^a   Schmidbauer, Patricia ^b   Kolanus, Waldemar ^c   Holzmann, Bernhard ^b   Grabbe, Stephan ^a   Laschinger, Melanie ^b  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

INTERCELLULAR ADHESION MOLECULE 1; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1;

ANIMAL CELL; ARTICLE; CELL ACTIVATION; CELL ADHESION; CELL INTERACTION; CELL PROLIFERATION; CONTROLLED STUDY; DELAYED HYPERSENSITIVITY; DENDRITIC CELL; IMMUNE RESPONSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TH1 CELL;

EID: 77956900499     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2009-05-224428     Document Type: Article

References (50)

1. Mempel TR, Henrickson SE, von Andrian UH. T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature. 2004;427(6979):154-159.
2. Miller MJ, Safrina O, Parker I, Cahalan MD. Imaging the single cell dynamics of CD4+ T cell activation by dendritic cells in lymph nodes. J Exp Med. 2004;200(7):847-856. (Pubitemid 39362921)
3. Stoll S, Delon J, Brotz TM, Germain RN. Dynamic imaging of T cell-dendritic cell interactions in lymph nodes. Science. 2002;296(5574):1873- 1876.
4. Bousso P, Robey E. Dynamics of CD8+ T cell priming by dendritic cells in intact lymph nodes. Nat Immunol. 2003;4(6):579-585. (Pubitemid 36701342)
5. Bachmann MF, Kall-Faienza K, Schmits R, et al. Distinct roles for LFA-1 and CD28 during activation of naive T cells: adhesion versus costimulation. Immunity. 1997;7(4):549-557.
6. Benvenuti F, Lagaudriere-Gesbert C, Grandjean I, et al. Dendritic cell maturation controls adhesion, synapse formation, and the duration of the interactions with naive T lymphocytes. J Immunol. 2004;172(1):292-301.
7. Scholer A, Hugues S, Boissonnas A, Fetler L, Amigorena S. Intercellular adhesion molecule-1-dependent stable interactions between T cells and dendritic cells determine CD8+ T cell memory. Immunity. 2008;28(2):258-270. (Pubitemid 351222655)
8. Varga G, Balkow S, Wild MK, et al. Active MAC-1 (CD11b/CD18) on DCs inhibits full T-cell activation. Blood. 2007;109(2):661-669.
9. Cambi A, Joosten B, Koopman M, et al. Organization of the integrin LFA-1 in nanoclusters regulates its activity. Mol Biol Cell. 2006;17(10):4270-4281.
10. Gunzer M, Weishaupt C, Hillmer A, et al. A spectrum of biophysical interaction modes between T cells and different antigen-presenting cells during priming in 3-D collagen and in vivo. Blood. 2004;104(9):2801-2809.
11. Luo BH, Carman CV, Springer TA. Structural basis of integrin regulation and signaling. Annu Rev Immunol. 2007;25:619-647. (Pubitemid 46697919)
12. Kolanus W, Nagel W, Schiller B, et al. Alpha L beta 2 integrin/LFA-1 binding to ICAM-1 induced by cytohesin-1, a cytoplasmic regulatory molecule. Cell. 1996;86(2):233-242.
13. Geiger C, Nagel W, Boehm T, et al. Cytohesin-1 regulates beta-2 integrin-mediated adhesion through both ARF-GEF function and interaction with LFA-1. EMBO J. 2000;19(11):2525-2536.
14. Weber KS, Weber C, Ostermann G, et al. Cytohesin-1 is a dynamic regulator of distinct LFA-1 functions in leukocyte arrest and transmigration triggered by chemokines. Curr Biol. 2001;11(24):1969-1974. (Pubitemid 33146424)
15. Boehm T, Hofer S, Winklehner P, et al. Attenuation of cell adhesion in lymphocytes is regulated by CYTIP, a protein which mediates signal complex sequestration. EMBO J. 2003;22(5):1014-1024.
16. Lu CF, Springer TA. The alpha subunit cytoplasmic domain regulates the assembly and adhesiveness of integrin lymphocyte function-associated antigen-1. J Immunol. 1997;159(1):268-278.
17. Semmrich M, Smith A, Feterowski C, et al. Importance of integrin LFA-1 deactivation for the generation of immune responses. J Exp Med. 2005;201(12):1987-1998.
18. Huser N, Fasan A, Semmrich M, et al. Intact LFA-1 deactivation promotes T-cell activation and rejection of cardiac allograft. Int Immunol. 2010;22(1):35-44.
19. Hogquist KA, Jameson SC, Heath WR, et al. T cell receptor antagonist peptides induce positive selection. Cell. 1994;76(1):17-27. (Pubitemid 24035278)
20. Scharffetter-Kochanek K, Lu H, Norman K, et al. Spontaneous skin ulceration and defective T cell function in CD18 null mice. J Exp Med. 1998;188(1):119-131.
21. Gunzer M, Schafer A, Borgmann S, et al. Antigen presentation in extracellular matrix: interactions of T cells with dendritic cells are dynamic, short lived, and sequential. Immunity. 2000;13(3):323-332.
22. Celli S, Lemaitre F, Bousso P. Real-time manipulation of T cell-dendritic cell interactions in vivo reveals the importance of prolonged contacts for CD4+ T cell activation. Immunity. 2007;27(4):625-634.
23. Alcover A, Alarcon B. Internalization and intracellular fate of TCR-CD3 complexes. Crit Rev Immunol. 2000;20(4):325-346.
24. Hofer S, Pfeil K, Niederegger H, et al. Dendritic cells regulate T-cell deattachment through the integrin-interacting protein CYTIP. Blood. 2006;107(3):1003-1009.
25. Quast T, Tappertzhofen B, Schild C, et al. Cytohesin-1 controls the activation of RhoA and modulates integrin-dependent adhesion and migration of dendritic cells. Blood. 2009;113(23):5801-5810.
26. Schlichting CL, Schareck WD, Weis M. Dendritic cell adhesion is enhanced on endothelial cells preexposed to calcineurin inhibitors. J Cardiovasc Pharmacol. 2005;46(3):250-254. (Pubitemid 41262824)
27. Grakoui A, Bromley SK, Sumen C, et al. The immunological synapse: a molecular machine controlling T cell activation. Science. 1999;285(5425):221- 227. (Pubitemid 29329988)
28. Skokos D, Shakhar G, Varma R, et al. Peptide-MHC potency governs dynamic interactions between T cells and dendritic cells in lymph nodes. Nat Immunol. 2007;8(8):835-844.
29. Henrickson SE, Mempel TR, Mazo IB, et al. T cell sensing of antigen dose governs interactive behavior with dendritic cells and sets a threshold for T cell activation. Nat Immunol. 2008;9(3):282-291.
30. Faroudi M, Zaru R, Paulet P, Muller S, Valitutti S. Cutting edge: T lymphocyte activation by repeated immunological synapse formation and intermittent signaling. J Immunol. 2003;171(3):1128-1132.
31. Bajenoff M, Wurtz O, Guerder S. Repeated antigen exposure is necessary for the differentiation, but not the initial proliferation, of naive CD4(+) T cells. J Immunol. 2002;168(4):1723-1729. (Pubitemid 34135770)
32. Celli S, Garcia Z, Bousso P. CD4 T cells integrate signals delivered during successive DC encounters in vivo. J Exp Med. 2005;202(9):1271-1278.
33. Carrasco YR, Fleire SJ, Cameron T, Dustin ML, Batista FD. LFA-1/ICAM-1 interaction lowers the threshold of B cell activation by facilitating B cell adhesion and synapse formation. Immunity. 2004;20(5):589-599.
34. Wang Y, Shibuya K, Yamashita Y, et al. LFA-1 decreases the antigen dose for T cell activation in vivo. Int Immunol. 2008;20(9):1119-1127.
35. Rothoeft T, Balkow S, Krummen M, et al. Structure and duration of contact between dendritic cells and T cells are controlled by T cell activation state. Eur J Immunol. 2006;36(12):3105-3117.
36. Geginat J, Bossi G, Bender JR, Pardi R. Anchorage dependence of mitogen-induced G1 to S transition in primary T lymphocytes. J Immunol. 1999;162(9):5085-5093. (Pubitemid 29307108)
37. Aszodi A, Hunziker EB, Brakebusch C, Fassler R. Beta1 integrins regulate chondrocyte rotation, G1 progression, and cytokinesis. Genes Dev. 2003;17(19):2465-2479.
38. Reverte CG, Benware A, Jones CW, LaFlamme SE. Perturbing integrin function inhibits microtubule growth from centrosomes, spindle assembly, and cytokinesis. J Cell Biol. 2006;174(4):491-497.
39. Schneider H, Downey J, Smith A, et al. Reversal of the TCR stop signal by CTLA-4. Science. 2006;313(5795):1972-1975.
40. Dustin ML, Bromley SK, Kan Z, Peterson DA, Unanue ER. Antigen receptor engagement delivers a stop signal to migrating T lymphocytes. Proc Natl Acad Sci U S A. 1997;94(8):3909-3913. (Pubitemid 27180472)
41. Morin NA, Oakes PW, Hyun YM, et al. Non-muscle myosin heavy chain IIA mediates integrin LFA-1 deadhesion during T lymphocyte migration. J Exp Med. 2008;205(1):195-205.
42. Ilani T, Vasiliver-Shamis G, Vardhana S, Bretscher A, Dustin ML. T cell antigen receptor signaling and immunological synapse stability require myosin IIA. Nat Immunol. 2009;10(5):531-539.
43. Sarris M, Andersen KG, Randow F, Mayr L, Betz AG. Neuropilin-1 expression on regulatory T cells enhances their interactions with dendritic cells during antigen recognition. Immunity. 2008;28(3):402-413.
44. Cher DJ, Mosmann TR. Two types of murine helper T cell clone, II: delayed-type hypersensitivity is mediated by TH1 clones. J Immunol. 1987;138(11):3688-3694.
45. Reichardt P, Dornbach B, Rong S, et al. Naive B cells generate regulatory T cells in the presence of a mature immunologic synapse. Blood. 2007;110(5):1519-1529.
46. van Gisbergen KP, Paessens LC, Geijtenbeek TB, van Kooyk Y. Molecular mechanisms that set the stage for DC-T cell engagement. Immunol Lett. 2005;97(2):199-208.
47. Lammermann T, Bader BL, Monkley SJ, et al. Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature. 2008;453(7191):51-55.
48. Burns S, Hardy SJ, Buddle J, et al. Maturation of DC is associated with changes in motile characteristics and adherence. Cell Motil Cytoskeleton. 2004;57(2):118-132. (Pubitemid 38134052)
49. Reichardt P, Dornbach B, Gunzer M. The molecular makeup and function of regulatory and effector synapses. Immunol Rev. 2007;218:165-177.
50. Watford WT, Li D, Agnello D, et al. Cytohesin binder and regulator (cybr) is not essential for T- and dendritic-cell activation and differentiation. Mol Cell Biol. 2006;26(17):6623-6632.